Comparative bone histology of rhabdodontid dinosaurs

Edina Prondvai

Cite this article: Prondvai E., 2014. Comparative bone histology of rhabdodontid dinosaurs. Palaeovertebrata 38 (2)-e1. doi: 10.18563/pv.38.2.e1

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Abstract

A comparative bone histological study of the three known genera of the endemic European ornithopod dinosaur family, Rhabdodontidae, is presented here in an ontogenetic context. Investigated specimens were assigned to different ontogenetic stages based exclusively on the histological indicators of osteologic maturation during diametrical bone growth; an entirely size-independent method as opposed to most previous studies. Qualitative comparison of bone histology of corresponding ontogenetic stages and elements among the three valid rhabdodontid genera, Mochlodon, Zalmoxes, and Rhabdodon, revealed some consistent patterns. Genus specific histological differences within Rhabdodontidae are most expressed between Rhabdodon and the Mochlodon-Zalmoxes clade. These indicate a prolonged phase of fast growth and a less constrained cyclicity in the growth dynamics of Rhabdodon, as opposed to the slower and more regulated growth strategy reflected in the bones of Mochlodon and Zalmoxes. These genus specific differences are consistent with the phylogenetic interrelation of the genera and are most probably related to the pronounced differences in body size. However, when compared to other ornithopods, most detected histological features in rhabdodontids do not seem to reliably reflect either phylogenetic relations or body size. A notable common feature of all rhabdodontid genera irrespective of body size is the ontogenetically early onset of cyclical growth and secondary remodelling; a pattern that more resembles the condition found in derived ornithopods than that described in more basal taxa which are closer relatives of rhabdodontids. The recognition of taxon-specific histological patterns as well as patterns indicative of ecological and thereby functional traits clearly requires more accurate, preferably quantitative evaluations.   

Bibliography

Allain, R., Pereda-Suberbiola, X., 2003. Dinosaurs of France. Comptes Rendus Palevol 2, 27-44. http://dx.doi.org/10.1016/S1631-0683(03)00002-2
 
Amling, M., Takeda, S., Karsenty, G., 2000. A neuro (endo)crine regulation of bone remodeling. BioEssays 22, 970-975. http://dx.doi.org/10.1002/1521-1878(200011)22:11<970::AID-BIES3>3.0.CO;2-L
 
Ascenzi, A., Bonucci, E., 1967. The tensile properties of single osteons. The Anatomical Record 158, 375-386. http://dx.doi.org/10.1002/ar.1091580403
 
Ascenzi, A., Bonucci, E., 1968. The compressive properties of single osteons. The Anatomical Record 158, 375-386. http://dx.doi.org/10.1002/ar.1091580403
 
Benton, M. J., Csiki, Z., Grigorescu, D., Redelstorff, R., Sander, P. M., Stein, K., Weishampel, D. B., 2010. Dinosaurs and the island rule: The dwarfed dinosaurs from Haţeg Island. Palaeogeography, Palaeoclimatology, Palaeoecology 293, 438-454. http://dx.doi.org/10.1016/j.palaeo.2010.01.026
 
Björndal, K., Bolten, A. B., Bennett, R. A., Jacobson, E. R., Wronski, T. J., Valeski, J. J., Elizar, P. J., 1998. Age and growth in sea turtles: limitations of skeletochronology for demographic studies. Copeia 1, 23-30. http://dx.doi.org/10.2307/1447698
 
Buffetaut, E., Cuny, G., Le Loeuff, J., 1993. The discovery of French dinosaurs. Modern Geology 18, 161-182.
 
Buffrénil, V. d., Castanet, J., 2000. Age estimation by skeletochronology in the Nile monitor (Varanus niloticus), a highly exploited species. Journal of Herpetology 34, 414-424. http://dx.doi.org/10.2307/1565365
 
Buffrénil, V. d., Houssaye, A., Böhme, W., 2008. Bone vascular supply in Monitor lizards (Squamata: Varanidae): influence of size, growth, and phylogeny. Journal of Morphology 269, 533-543. http://dx.doi.org/10.1002/jmor.10604
 
Bunzel, E., 1871. Die Reptilfauna der Gosau-Formation in der Neuen Welt bei Wiener-Neustadt. Abhandlungen der Kaiserlich-Königlichen geologischen Reichsanstalt 5, 1-18.
 
Castanet, J., Francillon-Vieillot, H., Meunier F., Ricqlès A. d., 1993. Bone and individual aging. In: Hall, B. K. (Ed.), Bones 7: Bone Growth. CRC Press, Ann Arbor, Michigan, pp. 245-283.
 
Chinsamy, A., 1993. Bone histology and growth trajectory of the prosauropod dinosaur Massospondylus carinatus Owen. Modern Geology 18, 319-329.
 
Chinsamy, A., 1995. Ontogenetic changes in the bone histology of the Late Jurassic ornithopod Dryosaurus lettowvorbecki. Journal of Vertebrate Paleontology 15(1), 96-104. http://dx.doi.org/10.1080/02724634.1995.10011209
 
Chinsamy, A., Rich, T., Vickers-Rich, P., 1998. Polar dinosaur bone histology. Journal of Vertebrate Paleontology 18(2), 385-390. http://dx.doi.org/10.1080/02724634.1998.10011066
 
Chinsamy-Turan, A., 2005. The microstructure of dinosaur bone: deciphering biology with fine-scale techniques. Johns Hopkins University Press, Baltimore.
 
Company, J., 2004. Vertebrados continentales del Cretácico Superior (Campaniense–Maastrichtiense) de València. PhD, Universitat de València.
 
Cormack, D. H., 1987. Ham’s histology. Lippincott William and Wilkins, New York.
 
Crockett, J., Rogers, M. J., Coxon, F. P., Hocking, L. J., Helfrich, M. H., 2011. Bone remodelling at a glance. Journal of Cell Science 124, 991-998. http://dx.doi.org/10.1242/jcs.063032
 
Cubo, J., Ponton, F., Laurin, M., Margerie, E. d., Castanet, J., 2005. Phylogenetic signal in bone microstructure of sauropsids. Systematic Biology 54(4), 562-574. http://dx.doi.org/10.1080/10635150591003461
 
Currey, J. D., 2003. The many adaptations of bone. Journal of Biomechanics 36, 1487-1495. http://dx.doi.org/10.1016/S0021-9290(03)00124-6
 
Curry, K. A., 1999. Ontogenetic histology of Apatosaurus (Dinosauria: Sauropoda): New insights on growth rates and longevity. Journal of Vertebrate Paleontology 19(4), 654-665. http://dx.doi.org/10.1080/02724634.1999.10011179
 
Enlow, D. H., 1962. A Study of the post-natal growth and remodeling of bone. American Journal of Anatomy 110(2), 79-101. http://dx.doi.org/10.1002/aja.1001100202
 
Erickson, G. M., 2005. Assessing dinosaur growth patterns: a microscopic revolution. Trends in Ecology and Evolution 20, 677-684. http://dx.doi.org/10.1016/j.tree.2005.08.012
 
Erickson, G. M., Tumanova, T. A., 2000. Growth curve of Psittacosaurus mongoliensis Osborn (Ceratopsia: Psittacosauridae) inferred from long bone histology. Zoological Journal of the Linnean Society 130, 551-566. http://dx.doi.org/10.1111/j.1096-3642.2000.tb02201.x
 
Erickson, G. M., Curry Rogers, K., Varricchio, D. J., Norell, M. A., Xu, X., 2007. Growth patterns in brooding dinosaurs reveal the timing of sexual maturity in non-avian dinosaurs and genesis of the avian condition. Biology Letters 3, 558-561. http://dx.doi.org/10.1098/rsbl.2007.0254
 
Erickson, G. M., Rauhut, O. W. M., Zhou, Z., Turner, A. H., Inouye, B. D., Hu, D., Norell, M. A., 2009. Was Dinosaurian Physiology Inherited by Birds? Reconciling slow growth in Archaeopteryx. PLoS ONE, 4(10), e7390, 1-9. http://dx.doi.org/10.1371/journal.pone.0007390
 
Esteban, M., García-París, M., Castanet, J., 1996. Use of bone histology in estimating the age of frogs (Rana perezi) from a warm temperate climate area. Canadian Journal of Zoology 74(10), 1914-1921. http://dx.doi.org/10.1139/z96-216
 
Francillon-Vieillot, H., Buffrénil, V. D., Castanet, J., Géraudie, J., Meunier, F. J., Sire, J. Y., Zylberberg, L., Ricqlès, A. d. 1990. Microstructure and mineralization of vertebrate skeletal tissues. In: Carter, J.G. (Ed.), Skeletal Biomineralization: Patterns, Processes and Evolutionary Trends. Van Nostrand Reinhold, New York, pp. 471-530.
 
Frost, H. M., 1969. Tetracycline-based histological analysis of bone remodeling. Calcified Tissue Research 3, 211-237. http://dx.doi.org/10.1007/BF02058664
 
Godefroit, P., Codrea, V., Weishampel, D. B., 2009. Osteology of Zalmoxes shqiperorum (Dinosauria, Ornithopoda), based on new specimens from the Upper Cretaceous of Nalat¸-Vad (Romania). Geodiversitas 31(3), 525-553. http://dx.doi.org/10.5252/g2009n3a3
 
Green, W. C. H., Rothstein, A., 1991. Trade-offs between growth and reproduction in female bison. Oecologia 86(4), 521-527. http://dx.doi.org/10.1007/BF00318318
 
Haines, W. R., 1942. The evolution of epiphyses and of endochondral bone. Biological Reviews 17(4), 267-292. http://dx.doi.org/10.1111/j.1469-185X.1942.tb00440.x
 
Horner, J. R., Ricqlès, A. d., Padian, K., 1999. Variation in dinosaur skeletochronology indicators: implications for age assessment and physiology. Paleobiology 25(3), 295-304.
 
Horner, J. R., Ricqlès, A. d., Padian, K., 2000. Long bone histology of the hadrosaurid dinosaur Maiasaura peeblesorum: growth dynamics and physiology based on an ontogenetic series of skeletal elements. Journal of Vertebrate Paleontology 20, 115-129. http://dx.doi.org/10.1671/0272-4634(2000)020[0115:LBHOTH]2.0.CO;2
 
Horner, J. R., Ricqlès, A. d., Padian, K., Scheetz, R. D., 2009. Comparative long bone histology and growth of the ‘‘hypsilophodontid’’ dinosaurs Orodromeus makelai, Dryosaurus altus, and Tenontosaurus tillettii (Ornithischia: Euornithopoda). Journal of Vertebrate Paleontology 29, 734-747. http://dx.doi.org/10.1671/039.029.0312
 
Hübner, T. R., 2012. Bone Histology in Dysalotosaurus lettowvorbecki (Ornithischia: Iguanodontia) - Variation, Growth, and Implications. PLoS ONE 7(1), e29958, 1-29. http://dx.doi.org/10.1371/journal.pone.0029958
 
Jakob, C., Seitz, A., Crivelli A. J., Miaud, C., 2002.  Growth cycle of the marbled newt (Triturus marmoratus) in the Mediterranean region assessed by skeletochronology. Amphibia-Reptilia 23(4), 407-418. http://dx.doi.org/10.1163/15685380260462329
 
Javed, A., Chen, H., Ghori, F. Y., 2010. Genetic and transcriptional control of bone formation. Oral and Maxillofacial Surgery Clinics of North America 22(3), 283-293. http://dx.doi.org/10.1016/j.coms.2010.05.001
 
Klein, N., Sander, M., 2008. Ontogenetic stages in the long bone histology of sauropod dinosaurs. Paleobiology 34, 248-264. http://dx.doi.org/10.1666/0094-8373(2008)034[0247:OSITLB]2.0.CO;2
 
Klein, N., Scheyer, T., Tütken, T., 2009. Skeletochronology and isotopic analysis of a captive individual of Alligator mississippiensis Daudin, 1802. Fossil Record 12(2), 121-131. http://dx.doi.org/10.5194/fr-12-121-2009
 
Köhler, M., Marín-Moratalla, N., Jordana, X., Aanes, R., 2012. Seasonal bone growth and physiology in endotherms shed light on dinosaur physiology. Nature 487, 358-361. http://dx.doi.org/10.1038/nature11264
 
Lee, A. H., Werning, S., 2008. Sexual maturity in growing dinosaurs does not fit reptilian growth models. Proceedings of the National Academy of Sciences USA 105, 582-587. http://dx.doi.org/10.1073/pnas.0708903105
 
Marotti, G., 2010. Static and dynamic osteogenesis. Italian Journal of Anatomy and Embryology 115, 123-126.
 
Matheron, P., 1869. Notice sur les reptiles fossiles des dépôts fluvio-lacustres crétacés du bassin à lignite de Fuveau. Extraits des Mémoires de l’Academie Impériale des
Sciences, Belles­Lettres et Arts de Marseilles 1869, 345-379.
 
Matsuki, T., Matsui, M., 2009. The validity of skeletochronology in estimating ages of Japanese Clouded Salamander, Hynobius nebulosus (Amphibia, Caudata). Current Herpetology 28(2), 41-48. http://dx.doi.org/10.3105/018.028.0201
 
McDonald, A. T., 2012. Phylogeny of basal iguanodonts (Dinosauria: Ornithischia): An update. PLoS ONE 7(5): e36745. http://dx.doi.org/10.1371/journal.pone.0036745
 
Nopcsa, F., 1902. Dinosaurierreste aus Siebenbürgen II. (Schädelreste von Mochlodon). Mit einem Anhange: zur Phylogenie der Ornithopodiden. Denkschriften der Kaiserlichen Akademie der Wissenschaften Wien 72, 149-175.
 
Ősi, A., Prondvai, E., Butler, R., Weishampel, D. B., 2012. Phylogeny, histology and inferred body size evolution in a new rhabdodontid dinosaur from the Late Cretaceous of Hungary. PLoS ONE 7(9), e44318. http://dx.doi.org/10.1371/journal.pone.0044318
 
Pereda-Suberbiola, X., Sanz, J. L., 1999. The ornithopod dinosaur Rhabdodon from the Upper Cretaceous of Lan˜o (Iberian Peninsula). Estudios del Museo de Ciencias Naturales de Alava 14: 257-272.
 
Pogoda, P., Priemel, M., Rueger J. M., Amling, M., 2005. Bone remodeling: new aspects of a key process that controls skeletal maintenance and repair. Osteoporosis International 16, S18-S24. http://dx.doi.org/10.1007/s00198-004-1787-y
 
Prondvai, E., Bodor, E. R., Ősi, A., 2014(b). Does morphology reflect osteohistology-based ontogeny? A case study of Late Cretaceous pterosaur jaw symphyses from Hungary reveals hidden taxonomic diversity. Paleobiology 40(2), 288-321. http://dx.doi.org/10.1666/13030
 
Prondvai, E., Stein, K. H. W., Ricqlès, A. d., Cubo, J., 2014(a). Development-based revision of bone tissue classification: the importance of semantics for science. Biological Journal of the Linnean Society 112, 799-816. http://dx.doi.org/10.1111/bij.12323
 
Reiss, M. J., 1989. The Allometry of Growth and Reproduction. Cambridge University Press, New York. http://dx.doi.org/10.1017/CBO9780511608483
 
Ricqlès, A. d., 1975. Recherches paléohistologiques sur les os longs des tétrapodes VII — Sur la classification, la signification fonctionelle et l’histoire des tissus osseux des tétrapodes. Première partie. Annales de Paléontologie 61, 51-129.
 
Sander, P.M., 2000. Long bone histology of the Tendaguru sauropods: implications for growth and biology. Paleobiology 26, 466-488. http://dx.doi.org/10.1666/0094-8373(2000)026<0466:LHOTTS>2.0.CO;2
 
Schmalhausen, I. I., 1949. Factors of evolution. University of Chicago Press, Chicago.
 
Seeley, H. G., 1881. The reptile fauna of the Gosau Formation preserved in the Geological Museum of the University of Vienna. With a note on the geological horizon of the fossils at Neue Welt, east of Wiener Neustadt. Quarterly Journal of the Geological Society, London 37, 620–707. http://dx.doi.org/10.1144/GSL.JGS.1881.037.01-04.49
 
Smith, K. K., 2001. Heterochrony revisited: the evolution of developmental sequences. Biological Journal of the Linnean Society 73, 169-186. http://dx.doi.org/10.1111/j.1095-8312.2001.tb01355.x
 
Stein, K., Prondvai, E., 2014. Rethinking the nature of fibrolamellar bone: an integrative biological revision of sauropod plexiform bone formation. Biological Reviews 89, 24-47. http://dx.doi.org/10.1111/brv.12041
 
Stein, K., Csiki, Z., Curry Rogers, K., Weishampel, D. B., Redelstorff, R., Sander, P. M., 2010. Small body size and extreme cortical bone remodeling indicate phyletic dwarfism in Magyarosaurus dacus (Sauropoda: Titanosauria). Proceedings of the National Academy of Sciences, USA 107, 9258-9263. http://dx.doi.org/10.1073/pnas.1000781107
 
Tortosa, T., Dutour, Y., Cheylan, G., Buffetaut, E., 2012. New discovery of titanosaurs (Dinosauria: Sauropoda) from Provence (SE France): implications on local paleobiodiversity. In: Royo-Torres, R., Gascó, F., Alcalá, L. (coord.), 10th Annual Meeting of the European Association of Vertebrate Palaeontologists. ¡Fundamental! 20, 259-262.
 
Varricchio, D. J., 1993. Bone microstructure of the Upper Cretaceous theropod dinosaur Troodon formosus. Journal of Vertebrate Paleontology 13, 99-104. http://dx.doi.org/10.1080/02724634.1993.10011490
 
Weishampel, D. B., Jianu, C. M., Csiki, Z., Norman, D. B., 2003. Osteology and phylogeny of Zalmoxes (n. g.), an unusual euornithopod dinosaur from the latest Cretaceous of Romania. Journal of Systematic Palaeontology 1, 65-123. http://dx.doi.org/10.1017/S1477201903001032
 
Wells, N. A., 1989. Making thin sections. In: Feldmann, R. M., Chapman, R. E., Hannibal J. T. (Eds.), Paleotechniques. University of Tennessee, Knoxville, pp. 120-129.
 
Werning, S., 2012. The ontogenetic osteohistology of Tenontosaurus tilletti. PLoS ONE 7(3), e33539. http://dx.doi.org/10.1371/journal.pone.0033539
 
Woodward, H. N., Rich, T. H., Chinsamy, A., Vickers-Rich, P., 2011. Growth dynamics of Australia’s polar dinosaurs. PLoS ONE 6(8), e23339. http://dx.doi.org/10.1371/journal.pone.0023339